Peripheral benzodiazepine receptor and its clinical targeting

Anti-Cancer Drugs

Volumn 15, Issue 8, 2004, Pages 737-745

  Decaudin, Didier ^a  

^a INSTITUT CURIE   (France)

Author keywords

Apoptosis; Cancer; Ligand; Mitochondria; Peripheral benzodiazepine receptor

Indexed keywords

ACETAMIDE DERIVATIVE; ANTINEOPLASTIC AGENT; BENZODIAZEPINE RECEPTOR; CERAMIDE GLUCOSYLTRANSFERASE INHIBITOR; DAUNORUBICIN; DEXAMETHASONE; ETOPOSIDE; GLUCOCORTICOID; IFOSFAMIDE; INDOLE DERIVATIVE; LIGAND; LONIDAMINE; MELPHALAN; MEMBRANE PROTEIN; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; PERMEABILITY TRANSITION PORE PROTEIN; PROTEIN BCL 2; RO 54864; SSR 180575; TAMOXIFEN; UNCLASSIFIED DRUG;

APOPTOSIS; CANCER THERAPY; CELL PROTECTION; DRUG EFFICACY; DRUG RECEPTOR BINDING; DRUG TARGETING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR CELL;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG DELIVERY SYSTEMS; FRANCE; HUMANS; NEOPLASMS; RECEPTORS, GABA-A;

EID: 4644224402     PISSN: 09594973     EISSN: None     Source Type: Journal    
DOI: 10.1097/00001813-200409000-00001     Document Type: Review

References (112)

1. Anholt RR, Pedersen PL, De Souza EB, Snyder SH. The peripheral-type benzodiazepine receptor. Localization to the mitochondrial outer membrane. J Biol Chem 1986; 261:576-583.
2. 3H]diazepam binding. Proc Natl Acad Sci USA 1977; 74:3805-3809.
3. Bernassau JM, Reversat JL, Ferrara P, Caput D, Lefur G. A 3D model of the peripheral benzodiazepine receptor and its implication in intra mitochondrial cholesterol transport. J Mol Graphics 1993; 11:236-245.
4. Olson JM, Ciliax BJ, Mancini WR, Young AB. Presence of peripheral-type benzodiazepine binding sites on human erythrocyte membranes. Eur J Pharmacol 1988; 152:47-53.
5. O'Beirne GB, Woods MJ, Williams DC. Two subcellular locations for peripheral-type benzodiazepine acceptors in rat liver. Eur J Biochem 1990; 188:131-138.
6. Hardwick M, Fertikh D, Culty M, Li H, Vidic B, Papadopoulos V. Peripheral-type benzodiazepine receptor (PBR) in human breast cancer: correlation of breast cancer cell aggressive phenotype with PBR expression, nuclear localization, and PBR-mediated cell proliferation and nuclear transport of cholesterol. Cancer Res 1999; 59:831-842.
7. Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim Biophys Acta 1995; 1241:139-176.
8. Kroemer G, Zamzami N, Susin SA. Mitochondrial control of apoptosis. Immunol Today 1997; 18:44-51.
9. Galiegue S, Jbilo O, Combes T, Bribes E, Carayon P, Le Fur G, et al. Cloning and characterization of PRAX-1. A new protein that specifically interacts with the peripheral benzodiazepine receptor. J Biol Chem 1999; 270:2938-2952.
10. Blahos 2nd J, Whalin ME, Krueger KE. Identification and purification of a 10-kilodalton protein associated with mitochondrial benzodiazepine receptors. J Biol Chem 1995; 270:20285-20291.
11. Li H, Yao Z, Degenhardt B, Teper G, Papadopoulos V. Cholesterol binding at the cholesterol recognition/interaction amino acid consensus (CRAC) of the peripheral-type benzodiazepine receptor and inhibition of steroidogenesis by an HIV TAT-CRAC peptide. Proc Natl Acad Sci USA 2001; 98:1267-1272.
12. West LA, Horvat RD, Roess DA, Barisas BG, Juengel JL, Niswender GD. Steroidogenic acute regulatory protein and peripheral-type benzodiazepine receptor associate at the mitochondrial membrane. Endocrinology 2001; 142:502-505.
13. Li H, Degenhardt B, Tobin D, Yao ZX, Tasken K, Papadopoulos V. Identification, localization, and function in steroidogenesis of PAP7: a peripheral-type benzodiazepine receptor- and PKA (RIalpha)-associated protein. Mol Endocrinol 2001; 15:2211-2228.
14. Everett H, Barry M, Lee SF, Sun X, Graham K, Stone J, et al. M11L: a novel mitochondria-localized protein of myxoma virus that blocks apoptosis of infected leukocytes. J Exp Med 2000; 191:1487-1498.
15. Moynagh PN, O'Neill LA, Williams DC. Interleukin-1 and phorbol myristate acetate modulate the peripheral-type benzodiazepine receptor in lymphocytes and glial cells. Biochem Pharmacol 1993; 46:821-827.
16. Itzhak Y, Norenberg MD. Regulation of peripheral-type benzodiazepine receptors in cultured astrocytes by monoamine and amino acid neurotransmitters. Brain Res 1994; 660:346-348.
17. Sridaran R, Philip GH, Li H, Culty M, Liu Z, Stocco DM, et al. GnRH agonist treatment decreases progesterone synthesis, luteal peripheral benzodiazepine receptor mRNA, ligand binding and Steroidogenic acute regulatory protein expression during pregnancy. J Mol Endocrinol 1999; 22:45-54.
18. Rey C, Mauduit C, Naureils O, Benahmed M, Louisot P, Gasnier F. Upregulation of mitochondrial peripheral benzodiazepine receptor expression by tumor necrosis factor alpha in testicular leydig cells. Possible involvement in cell survival. Biochem Pharmacol 2000; 60:1639-1646.
19. Golani I, Weizman A, Leschiner S, Spanier I, Eckstein N, Limor R, et al. Hormonal regulation of peripheral benzodiazepine receptor binding properties is mediated by subunit interaction. Biochemistry 2001; 40:10213-10222.
20. Trincavelli ML, Marselli L, Falleni A, Gremigni V, Ragge E, Dotta F, et al. Upregulation of mitochondrial peripheral benzodiazepine receptor expression by cytokine-induced damage of human pancreatic islets. J Cell Biochem 2002; 84:636-644.
21. 3H]PK11195 binding in gerbil hippocampus after transient forebrain ischemia. J Neurosci Res 2001; 64:493-500.
22. Hauet T, Han Z, Wang Y, Hameury F, Jayle C, Gibelin H, et al. Modulation of peripheral-type benzodiazepine receptor levels in a reperfusion injury pig kidney-graft model. Transplantation 2002; 74:1507-1515.
23. Mazzone A, Mazzucchelli I, Vezzoli M, Ottini E, Auguadro C, Serio A, et al. Increased expression of peripheral benzodiazepine receptors on leukocytes in silent myocardial ischemia. J Am Coll Cardiol 2000; 36:746-750.
24. Kuhlmann AC, Guilarte TR. Regional and temporal expression of the peripheral benzodiazepine receptor in MPTP neurotoxicity. Toxicol Sci 1999; 48:107-116.
25. Hazell AS, Normandin L, Nguyen B, Kennedy G. Upregulation of 'peripheral-type' benzodiazepine receptors in the globus pallidus in a sub-acute rat model of manganese neurotoxicity. Neurosci Lett 2003; 349:13-16.
26. Mankowski JL, Queen SE, Tarwater PJ, Adams RJ, Guilarte TR. Elevated peripheral benzodiazepine receptor expression in simian immunodeficiency virus encephalitis. J Neurovirol 2003; 9:94-100.
27. Haussinger D, Schliess F, Kircheis G. Pathogenesis of hepatic encephalopathy. J Gastroenterol Hepatol 2002; 17:S256-S259.
28. Sauvageau A, Desjardins P, Lozeva V, Rose C, Hazell AS, Bouthillier A, et al. Increased expression of 'peripheral-type' benzodiazepine receptors in human temporal lobe epilepsy: implications for PET imaging of hippocampal sclerosis. Metab Brain Dis 2002; 17:3-11.
29. Lacor P, Gandolfo P, Tonon MC, Brault E, Dalibert I, Schumacher M, et al. Regulation of the expression of peripheral benzodiazepine receptors and their endogenous ligands during rat sciatic nerve degeneration and regeneration: a role for PBR in neurosteroidogenesis. Brain Res 1999; 815:70-80.
30. Raghavendra Rao VL, Dogan A, Bowen KK, Dempsey RJ. Traumatic brain injury leads to increased expression of peripheral-type benzodiazepine receptors, neuronal death, and activation of astrocytes and microglia in rat thalamus. Exp Neurol 2000; 161:102-114.
31. Lukeman DS, Vaughn DA, Fanestil DD. Selective pharmacological modulation of renal peripheral-type benzodiazepine binding by treatment with diuretic drugs. Life Sci 1988; 42:367-373.
32. Leschiner S, Weizman R, Shoukrun R, Veenman L, Gavish M. Tissue-specific regulation of the peripheral benzodiazepine receptor by antidepressants and lithium. Neuropsychobiology 2000; 42:127-134.
33. Zavala F, Veber F, Descamps-Latscha B. Altered expression of neutrophil peripheral benzodiazepine receptor in X-linked chronic granulomatous disease. Blood 1990; 76:184-188.
34. Zavala F, Veber F, Taupin V, Nguyen AT, Descamps-Latscha B. Reconstitution of peripheral benzodiazepine receptor expression in X-linked chronic granulomatous disease by interferon-gamma. Lancet 1990; 336:758-759.
35. Carmel I, Fares FA, Leschiner S, Scherubl H, Weisinger G, Gavish M. Peripheral-type benzodiazepine receptors in the regulation of proliferation of MCF-7 human breast carcinoma cell line. Biochem Pharmacol 1999; 58:273-278.
36. Beinlich A, Strohmeier R, Kaufmann M, Kuhl H. Relation of cell proliferation to expression of peripheral benzodiazepine receptors in human breast cancer cell lines. Biochem Pharmacol 2000; 60:397-402.
37. Papadopoulos V, Kapsis A, Li H, Amri H, Hardwick M, Culty M, et al. Drug-induced inhibition of the peripheral-type benzodiazepine receptor expression and cell proliferation in human breast cancer cells. Anticancer Res 2000; 20:2835-2847.
38. Sanger N, Strohmeier R, Kaufmann M, Kuhl H. Cell cycle-related expression and ligand binding of peripheral benzodiazepine receptor in human breast cancer cell lines. Eur J Cancer 2000; 36:2157-2163.
39. Strohmeier R, Roller M, Sanger N, Knecht R, Kuhl H. Modulation of tamoxifen-induced apoptosis by peripheral benzodiazepine receptor ligands in breast cancer cells. Biochem Pharmacol 2002; 64:99-107.
40. Hardwick M, Cavalli LR, Barlow KD, Haddad BR, Papadopoulos V. Peripheral-type benzodiazepine receptor (PBR) gene amplification in MDA-MB-231 aggressive breast cancer cells. Cancer Genet Cytogenet 2002; 139:48-51.
41. Papadopoulos V, Amri H, Li H, Boujrad N, Vidic B, Gamier M. Targeted disruption of the peripheral-type benzodiazepine receptor gene inhibits steroidogenesis in the R2C Leydig tumor cell line. J Biol Chem 1997; 272:32129-32135.
42. Rao RM, Jo Y, Babb-Tarbox M, Syapin PJ, Stocco DM. Regulation of steroid hormone biosynthesis in R2C and MA-10 Leydig tumor cells: role of the cholesterol transfer proteins StAR and PBR. Endocr Res 2002; 28:387-394.
43. Sutler AP, Maaser K, Hopfner M, Barthel B, Grabowski P, Faiss S, et al. Specific ligands of the peripheral benzodiazepine receptor induce apoptosis and cell cycle arrest in human esophageal cancer cells. Int J Cancer 2002; 102:318-327.
44. Maaser K, Hopfner M, Jansen A, Weisinger G, Gavish M, Kozikowski AP, et al. Specific ligands of the peripheral benzodiazepine receptor induce apoptosis and cell cycle arrest in human colorectal cancer cells. Br J Cancer 2001; 85:1771-1780.
45. Thompson WE, Branch A, Whittaker JA, Lyn D, Zilberstein M, Mayo KE, et al. Characterization of prohibitin in a newly established rat ovarian granulosa cell line. Endocrinology 2001; 142:4076-4085.
46. Decaudin D, Castedo M, Nemati F, Beurdeley-Thomas A, De Pinieux G, Caron A, et al. Peripheral benzodiazepine receptor ligands reverse apoptosis resistance of cancer cells in vitro and in vivo. Cancer Res 2002; 62:388-393.
47. Batra S, Alenfall J. Characterization of peripheral benzodiazepine receptors in rat prostatic adenocarcinoma. Prostate 1994; 24:269-278.
48. Whittle IR, Kelly PA. Mechanisms of peritumoural brain dysfunction: metabolic and neuroreceptor findings in striatal C6 glioma. J Clin Neurosci 2001; 8:430-434.
49. Venturini I, Zeneroli ML, Corsi L, Avallone R, Farina F, Alho H, et al. Upregulation of peripheral benzodiazepine receptor system in hepatocellular carcinoma. Life Sci 1998; 63:1269-1280.
50. Batra S, Iosif CS. Elevated concentrations of mitochondrial peripheral benzodiazepine receptors in ovarian tumors. Int J Oncol 1998; 12:1295-1298.
51. Miettinen H, Kononen J, Haapasalo H, Helen P, Sallinen P, Harjuntausta T, et al. Expression of peripheral-type benzodiazepine receptor and diazepam binding inhibitor in human astrocytomas: relationship to cell proliferation. Cancer Res 1995; 55:2691-2695.
52. Batra S, Iosif CS. Peripheral benzodiazepine receptor in human endometrium and endometrial carcinoma. Anticancer Res 2000; 20:463-466.
53. Maaser K, Grabowski P, Sutter AP, Hopfner M, Foss HD, Stein H, et al. Overexpression of the peripheral benzodiazepine receptor is a relevant prognostic factor in stage III colorectal cancer. Clin Cancer Res 2002; 8:3205-3209.
54. Garnier M, Boujrad N, Ogwuegbu SO, Hudson Jr JR, Papadopoulos V. The polypeptide diazepam-binding inhibitor and a higher affinity mitochondrial peripheral-type benzodiazepine receptor sustain constitutive steroidogenesis in the R2C Leydig tumor cell line. J Biol Chem 1994; 269:22105-22112.
55. Tsankova V, Magistrelli A, Cantoni L, Tacconi MT. Peripheral benzodiazepine receptor ligands in rat liver mitochondria: effect on cholesterol translocation. Eur J Pharmacol 1997; 294:601-607.
56. Li H, Papadopoulos V. Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern. Endocrinology 1998; 139:4991-4997.
57. Papadopoulos V, Widmaier EP, Amri H, Zilz A, Li H, Culty M, et al. In vivo studies on the role of the peripheral benzodiazepine receptor (PBR) in steroidogenesis. Endocr Res 1998; 24:479-487.
58. Culty M, Li H, Boujrad N, Amri H, Vidic B, Bernassau JM, et al. In vitro studies on the role of the peripheral-type benzodiazepine receptor in steroidogenesis. J Steroid Biochem Mol Biol 1999; 69:123-130.
59. Lacapere JJ, Papadopoulos V. Peripheral-type benzodiazepine receptor: structure and function of a cholesterol-binding protein in steroid and bile acid biosynthesis. Steroids 2003; 68:569-585.
60. Delavoie F, Li H, Hardwick M, Robert JC, Giatzakis C, Peranzi G, et al. In vivo and in vitro peripheral-type benzodiazepine receptor polymerization: functional significance in drug ligand and cholesterol binding. Biochemistry 2003; 42:4506-4519.
61. Hauet T, Liu J, Li H, Gazouli M, Culty M, Papadopoulos V. PBR, StAR, and PKA: partners in cholesterol transport in steroidogenic cells. Endocr Res 2002; 28:395-401.
62. Lacor P, Gandolfo P, Tonon MC, Brault E, Dalibert I, Schumacher M, et al. Regulation of the expression of peripheral benzodiazepine receptors and their endogenous ligands during rat sciatic nerve degeneration and regeneration: a role for PBR in neurosteroidogenesis. Brain Res 1999; 815:70-80.
63. Lang S. The role of peripheral benzodiazepine receptors (PBRs) in CNS pathophysiology. Curr Med Chem 2002; 9:1411-1415.
64. Papadopoulos V. Peripheral benzodiazepine receptor: structure and function in health and disease. Ann Pharm Fr 2003; 61:30-50.
65. Cascio C, Brown RC, Liu Y, Han Z, Hales DB, Papadopoulos V. Pathways of dehydroepiandrosterone formation in developing rat brain glia. J Steroid Biochem Mol Biol 2000; 75:177-186.
66. McGeer EG, Singh EA, McGeer PL. Peripheral-type benzodiazepine binding in Alzheimer disease. Alzheim Dis AssDisord 1988; 2:331-336.
67. Messmer K, Reynolds GP. Increased peripheral benzodiazepine binding sites in the brain of patients with Huntington's disease. Neurosci Lett 1998; 241:53-56.
68. Cagnin A, Brooks DJ, Kennedy AM, Gunn RN, Myers R, Turkheimer FE, et al. In-vivo measurement of activated microglia in dementia. Lancet 2001; 359:461-467.
69. Brown RC, Han Z, Cascio C, Papadopoulos V. Neurosteroids: oxidative stress mediated dehydroepiandrosterone formation in Alzheimer's disease pathology. Neurobiol Aging 2003; 24:57-65.
70. Laird HE II, Gerrish KE, Duerson KC, Putnam CW, Russell DH. Peripheral benzodiazepine binding sites in Nb 2 node lymphoma cells: effects on prolactin-stimulated proliferation and ornithine decarboxylase activity. Eur J Pharmacol 1989; 171:25-35.
71. Garnier M, Boujrad N, Oke BO, Brown AS, Riond J, Ferrara P, et al. Diazepam binding inhibitor is a paracrine/autocrine regulator of Leydig cell proliferation and steroidogenesis: action via peripheral-type benzodiazepine receptor and independent mechanisms. Endocrinology 1993; 132:444-458.
72. Camins A, Diez-Fernandez C, Pujadas E, Camarasa J, Escubedo E. A new aspect of the antiproliferative action of peripheral-type benzodiazepine receptor ligands. Eur J Pharmacol 1995; 272:289-292.
73. Neary JT, Jorgensen SL, Oracion A, Bruce JH, Norenberg MD. Inhibition of growth factor-induced DNA synthesis in astrocytes by ligands of peripheral-type benzodiazepine receptors. Brain Res 1995; 675:27-30.
74. Landau M, Weizman A, Zoref-Shani E, Beery E, Wasseman L, Landau O, et al. Antiproliferative and differentiating effects of benzodiazepine receptor ligands on B16 melanoma cells. Biochem Pharmacol 1998; 56:1029-1034.
75. Hardwick M, Rone J, Man Z, Haddad B, Papadopoulos V. Peripheral-type benzodiazepine receptor levels correlate with the ability of human breast cancer MDA-MB-231 cell line to grow in SCID mice. Int J Cancer 2001; 94:322-327.
76. Brown RC, Degenhardt B, Kotoula M, Papadopoulous V. Location-dependent role of the human glioma cell peripheral-type benzodiazepine receptor in proliferation and steroid biosynthesis. Cancer Lett 2000; 156:125-132.
77. Coleman PS, Chen LC, Sepp-Lorenzino L. Cholesterol metabolism and tumor cell proliferation. In: Bittman R (editor): Cholesterol: Its Functions and Metabolism in Biology and Medicine. New York: Renum; 1997, pp. 363-435.
78. Torres SR, Frode TS, Nardi GM, Vita N, Reeb R, Ferrara P, et al. Anti-inflammatory effects of peripheral benzodiazepine receptor ligands in two mouse models of inflammation. Eur J Pharmacol 2000; 408:199-211.
79. Waterfield JD, McGeer EG, McGeer PL. The peripheral benzodiazepine receptor ligand PK11195 inhibits arthritis in the MRL-lpr mouse model. Rheumatology 1999; 38:1068-1073.
80. Bribes E, Bourrie B, Esclangon M, Galiegue S, Vidai H, Casellas P. Involvement of the peripheral benzodiazepine receptor in the development of rheumatoid arthritis in Mrl/lpr mice. Eur J Pharmacol 2002; 452:111-122.
81. Bessler H, Caspi B, Gavish M, Rehavi M, Hart J, Weizman R. Peripheral-type benzodiazepine receptor ligands modulate human natural killer cell activity. Int J Immunopharmacol 1997; 19:249-254.
82. Camins A, Diez-Fernandez C, Camarasa J, Escubedo E. Cell surface expression of heat shock proteins in dog neutrophils induced by mitochondrial benzodiazepine receptor ligands. Immunopharmacology 1995; 29:159-166.
83. Canat X, Guillaumont A, Bouaboula M, Poinot-Chazel C, Derocq JM, Carayon P, et al. Peripheral benzodiazepine receptor modulation with phagocyte differentiation. Biochem Pharmacol 1993; 46:551-554.
84. Marino F, Cattaneo S, Cosentino M, Rasini E, Di Grazia L, Fietta AM, et al. Diazepam stimulates migration and phagocytosis of human neutrophils: possible contribution of peripheral-type benzodiazepine receptors and intracellular calcium. Pharmacology 2001; 63:42-49.
85. Sacerdote P, Locatelli LD, Panerai AE. Benzodiazepine induced chemotaxis of human monocytes: a tool for the study of benzodiazepine receptors. Life Sci 1993; 53:653-658.
86. Galiegue S, Tinel N, Casellas P. The peripheral benzodiazepine receptor: a promising therapeutic drug target. Curr Med Chem 2003; 10:1563-1572.
87. Leducq N, Bono F, Sulpice T, Vin V, Janiak P, Fur GL, et al. Role of peripheral benzodiazepine receptors in mitochondrial, cellular, and cardiac damage induced by oxidative stress and ischemia-reperfusion. J Pharmacol Exp Ther 2003; 306:828-837.
88. Carayon P, Portier M, Dussossoy D, Bord A, Petitpretre G, Canat X, et al. Involvement of peripheral benzodiazepine receptors in the protection of hematopoietic cells against oxygen radical damage. Blood 1996; 87:3170-3178.
89. Miccoli L, Oudard S, Beurdeley-Thomas A, Dutrillaux B, Poupon MF. Effect of 1-(2-chlorophenyl)-N-methyl-N-(1-methylpropyl)-3-isoquinoline carboxamide (PK11195), a specific ligand of the peripheral benzodiazepine receptor, on the lipid fluidity of mitochondria in human glioma cells. Biochem Pharmacol 1999; 58:715-721.
90. Pelaia G, Di Paola ED, De Sarro G, Marsico SA. Is the mitochondrial benzodiazepine receptor involved in the control of airway smooth muscle tone? Gen Pharmacol 1997; 28:495-498.
91. Nakajima O, Hashimoto Y, Iwasaki S. Possible involvement of peripheral-type benzodiazepine receptors in erythroid differentiation of human leukemia cell line, K562. Biol Pharm Bull 1995; 18:903-906.
92. Taketani S, Kohno H, Okuda M, Furukawa T, Tokunaga R. Induction of peripheral-type benzodiazepine receptors during differentiation of mouse erythroleukemia cells. A possible involvement of these receptors in heme biosynthesis. J Biol Chem 1994; 269:7527-7531.
93. Taketani S, Kohno H, Furukawa T, Tokunaga R. Involvement of peripheral-type benzodiazepine receptors in the intracellular transport of heme and porphyrins. J Biochem (Tokyo) 1995; 117:875-880.
94. Susin SA, Zamzami N, Castedo M, Daugas E, Wang HG, Geley S, et al. The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95- and ceramide-induced apoptosis. J Exp Med 1997; 186:25-37.
95. Kroemer G. Mitochondrial control of apoptosis: an introduction. Biochem Biophys Res Com 2003; 304:433-435.
96. Ravagnan L, Roumier T, Kroemer G. Mitochondria - the killer organelles and their weapons. J Cell Physiol 2002; 192:131-137.
97. Stoebner PE, Carayon P, Penarier G, Frechin N, Barneon G, Casellas P, et al. The expression of peripheral benzodiazepine receptors in human skin: the relationship with epidermal cell differentiation. Br J Dermatol 1999; 140:1010-1016.
98. Casellas P, Galiegue S, Basile AS. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem Int 2002; 40:475-486.
99. Patterson S, Spahr CS, Daugas E, Susin SA, Irinopoulou T, Koehler C, et al. Mass spectrometric identification of proteins released from mitochondria undergoing permeability transition. Cell Death Differ 2000; 7:137-144.
100. Everett H, Barry M, Sun X, Lee SF, Frantz C, Berthiaume LG, et al. The myxoma provirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore. J Exp Med 2002; 196:1127-1139.
101. Kupczyk-Subotkowska L, Siahaan TJ, Basile AS, Friedman HS, Higgins PE, Song D, et al. Modulation of melphalan resistance in glioma cells with a peripheral benzodiazepine receptor ligand-melphalan conjugate. J Med Chem 1997; 40:1726-1730.
102. Hirsch T, Decaudin D, Susin SA, Marchetti P, Larochette N, Resche-Rigon M, et al. PK11195, a ligand of the mitochondrial benzodiazepine receptor, facilitates the induction of apoptosis and reverses Bcl-2-mediated cytoprotection. Exp Cell Res 1998; 241:426-434.
103. Miccoli L, Poirson-Bichat F, Sureau F, Bras Goncalves R, Bourgeois Y, Dutrillaux B, et al. Potentiation of lonidamine and diazepam, two agents acting on mitochondria, in human glioblastoma treatment. J Natl Cancer Inst 1998; 90:1400-1406.
104. Bono F, Lamarche I, Prabonnaud V, Le Fur G, Herbert JM. Peripheral benzodiazepine receptor agonists exhibit potent antiapoptotic activities. Biochem Biophys Res Commun 1999; 265:457-461.
105. Tanimoto Y, Onishi Y, Sato Y, Kizaki H. Benzodiazepine receptor agonists modulate thymocyte apoptosis through reduction of the mitochondrial transmembrane potential. Jpn J Pharmacol 1999; 79:177-183.
106. Kessel D, Antolovich M, Smith KM. The role of the peripheral benzodiazepine receptor in the apoptotic response to photodynamic therapy. Photochem Photobiol 2001; 74:346-349.
107. Banker DE, Cooper JJ, Fennell DA, Willman CL, Appelbaum FR, Cotter FE. PK11195, a peripheral benzodiazepine receptor ligand, chemosensitizes acute myeloid leukemia cells to relevant therapeutic agents by more than one mechanism. Leuk Res 2002; 26:91-106.
108. Jakubikova J, Duraj J, Hunakova L, Chorvath B, Sedlak J. PK11195, an isoquinoline carboxamide ligand of the mitochondrial benzodiazepine receptor, increased drug uptake and facilitated drug-induced apoptosis in human multidrug-resistant leukemia cells in vitro. Neoplasma 2002; 49:231-236.
109. Morris RL, Varnes ME, Kenney ME, Li YS, Azizuddin K, McEnery MW, et al. The peripheral benzodiazepine receptor in photodynamic therapy with the phthalocyanine photosensitizer Pc 4. Photochem Photobiol 2002; 75:652-661.
110. Sutler AP, Maaser K, Barthel B, Scherubl H. Ligands of the peripheral benzodiazepine receptor induce apoptosis and cell cycle arrest in oesophageal cancer cells: involvement of the p38MAPK signalling pathway. Br J Cancer 2003; 89:564-572.
111. 3H]PK11195, by thermodynamic studies. Life Sci 1983; 33:449-457.
112. Costantini P, Jacotot E, Decaudin D, Kroemer G. Mitochondrion as a novel target of anticancer chemotherapy. J Natl Cancer Inst 2000; 92:1042-1053.